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Multifunctional Properties of Chicken Embryonic Prenatal Mesenchymal Stem Cells- Pluripotency, Plasticity, and Tumor Suppression

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Abstract

The chick embryo represents an accessible and economical in vivo model, which has long been used in developmental biology, gene expression analysis, and loss/gain of function experiments. In the present study, we assessed and characterized bone marrow derived mesenchymal stem cells from prenatal day 13 chicken embryos (chBMMSCs) and determined some novel properties. After assessing the mesenchymal stem cell (MSC) properties of these cells by the presence of their signature markers (CD 44, CD 73, CD 90, CD 105, and vimentin), we ascertained a very broad spectrum of multipotentiality as these MSCs not only differentiated into the classic tri-lineages of MSCs but also into ectodermal, endodermal, and mesodermal lineages such as neuron, hepatocyte, islet cell, and cardiac. In addition to wide plasticity, we detected the presence of several pluripotent markers such as Oct4, Sox2, and Nanog. This is the first study characterizing prenatal chBMMSCs and their ability to not only differentiate into mesenchymal lineages but also into all the germ cell layer lineages. Furthermore, our studies indicate that prenatal chBMMSCs derived from the chick provide an excellent model for multi-lineage development studies because of their broad plasticity and faithful reproduction of MSC traits as seen in the human. Here, we also present evidence for the first time that media derived from prenatal chBMMSC cultures have an anti-tumorigenic, anti-migratory, and pro-apoptotic effect on human tumors cells acting through the Wnt-ß-catenin pathway. These data confirm that chBMMSCs are enriched with factors in their secretome that are able to destroy tumor cells. This suggests a commonality of properties of MSCs across species between human and chicken.

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References

  1. Arthur, A., Rychkov, G., Shi, S., Koblar, S. A., & Gronthos, S. (2008). Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells, 26, 1787–1795.

    Article  CAS  PubMed  Google Scholar 

  2. Sigurjonsson, O. E., Perreault, M. C., Egeland, T., & Glover, J. C. (2005). Adult human hematopoietic stem cells produce neurons efficiently in the regenerating chicken embryo spinal cord. Proceeding of the Natational Academy Sciences of the U S A., 102, 5227–5232.

    Article  CAS  Google Scholar 

  3. Murrell, W., Féron, F., Wetzig, A., Cameron, N., Splatt, K., Bellette, B., Bianco, J., Perry, C., Lee, G., & Mackay-Sim, A. (2005). Multipotent stem cells from adult olfactory mucosa. Developmental Dynamics, 233, 496–515.

    Article  PubMed  Google Scholar 

  4. Park, T. S., Zambidis, E. T., Lucitti, J. L., Logar, A., Keller, B. B., & Péault, B. (2009). Human embryonic stem cell-derived hematoendothelial progenitors engraft chicken embryos. Experimental Hematology, 37, 31–41.

    Article  CAS  PubMed  Google Scholar 

  5. Jadlowiec, J., Dongell, D., Smith, J., Conover, C., & Campbell, P. (2005). Pregnancy-associated plasma protein-a is involved in matrix mineralization of human adult mesenchymal stem cells and angiogenesis in the chick chorioallantoic membrane. Endocrinology, 146, 3765–3772.

    Article  CAS  PubMed  Google Scholar 

  6. Pisati, F., Belicchi, M., Acerbi, F., Marchesi, C., Giussani, C., Gavina, M., Javerzat, S., Hagedorn, M., Carrabba, G., Lucini, V., Gaini, S. M., Bresolin, N., Bello, L., Bikfalvi, A., & Torrente, Y. (2007). Effect of human skin-derived stem cells on vessel architecture, tumor growth, and tumor invasion in brain tumor animal models. Cancer Research, 67, 3054–3063.

    Article  CAS  PubMed  Google Scholar 

  7. Khatri, M., O’Brien, T. D., & Sharma, J. M. (2009). Isolation and differentiation of chicken mesenchymal stem cells from bone marrow. Stem Cells and Development, 18, 1485–92.

    Article  CAS  PubMed  Google Scholar 

  8. Rengaraj, D., Zheng, Y. H., Kang, K. S., Park, K. J., Lee, B. R., Lee, S. I., Choi, J. W., & Han, J. J. (2010). Conserved expression pattern of chicken DAZL in primordial germ cells and germ-line cells. Theriogenology, 74(5), 765–776.

    Article  CAS  PubMed  Google Scholar 

  9. Warrier, S., Haridas, N., & Bhonde, R. (2012). Inherent propensity of amnion derived mesenchymal stem cells towards endothelial lineage: vascularization from an avascular tissue. Placenta, 33, 850–858.

    Article  CAS  PubMed  Google Scholar 

  10. Mather, J. P., & Roberts, P. E. (1998). Introduction to Cell and Tissue Culture: Theory and Technique. New York: Plenum Press.

    Google Scholar 

  11. Wang, X., Hisha, H., Taketani, S., Adachi, Y., Li, Q., Cui, W., Cui, Y., Wang, J., Song, C., Mizokami, T., Okazaki, S., Li, Q., Fan, T., Fan, Z., Ershwin, E., & Ikehara, S. (2005). Characterization of mesenchymal stem cells isolated from mouse fetal bone marrow. Stem Cells, 24, 482–93.

    Article  CAS  PubMed  Google Scholar 

  12. Hung, S. C., Chen, N. J., Hsieh, S. L., Li, H., Ma, H. L., & Lo, W. H. (2002). Isolation and characterization of size-sieved stem cells from human bone marrow. Stem Cells, 20, 249–258.

    Article  PubMed  Google Scholar 

  13. Xiao, Y., Qian, H., Young, W. G., & Bartold, P. M. (2003). Tissue engineering for bone regeneration using differentiated alveolar bone cells in collagen scaffolds. Tissue Engineering, 9, 1167–1177.

    Article  CAS  PubMed  Google Scholar 

  14. Seo, M. J., Suh, S. Y., Bae, Y. C., & Jung, J. S. (2005). Differentiation of human adipose stromal cells into hepatic lineage in vitro and in vivo. Biochemical and Biophysical Research Communications, 328, 258–64.

    Article  CAS  PubMed  Google Scholar 

  15. Chen, L. B., Jiang, X. B., & Yang, L. (2004). Differentiation of rat marrow mesenchymal stem cells into pancreatic islet beta-cells. World Journal of Gastroenterology, 10, 3016–20.

    CAS  PubMed  Google Scholar 

  16. Woodbury, D., Reynolds, K., & IB Black, I. B. (2002). Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. Journal of Neuroscience Research, 69, 908–17.

    Article  CAS  PubMed  Google Scholar 

  17. Kim, B. J., Seo, J. H., Bubien, J. K., & Oh, Y. S. (2002). Differentiation of adult bone marrow stem cells into neuroprogenitor cells in vitro. Neuroreport, 13, 1185–1188.

    Article  PubMed  Google Scholar 

  18. Yang, G., Tian, J., Feng, C., Zhao, L., Liu, Z., & Zhu, J. (2012). Trichostatin a promotes cardiomyocyte differentiation of Rat mesenchymal stem cells after 5-azacytidine induction or during coculture with neonatal cardiomyocytes via a mechanism independent of histone deacetylase inhibition. Cell Transplantation, 21, 985–996.

    Article  PubMed  Google Scholar 

  19. Donovan, D., Brown, N. J., Bishop, E. T., & Lewis, C. E. (2001). Comparison of three in vitro human ‘angiogenesis’ assays with capillaries formed in vivo. Angiogenesis, 4(2), 113–21.

    Article  CAS  PubMed  Google Scholar 

  20. Liang, C. C., Park, A. Y., & Guan, J. L. (2007). In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nature Protocols, 2, 329–333.

    Article  CAS  PubMed  Google Scholar 

  21. Constantinou, T. F., Baumann, D., Lacher, M., Saurer, S., Friis, R., & Dharmarajan, A. (2008). SFRP-4 abrogates Wnt-3a-induced β-catenin and Akt/PKB signalling and reverses a Wnt-3a-imposed inhibition of in vitro mammary differentiation. Journal of Molecular Signaling, 3, 10.

    Article  PubMed Central  PubMed  Google Scholar 

  22. Martin, I., Padera, R. F., Vunjak-Novakovic, G., & Freed, L. E. (1998). In vitro differentiation of chick embryo bone marrow stromal cells into cartilaginous and bone-like tissues. Journal of Orthopaedic Research, 16(2), 181–9.

    Article  CAS  PubMed  Google Scholar 

  23. Bai, C., Hou, L., Ma, Y., Chen, L., Zhang, M., & Guan, W. (2013). Isolation and characterization of mesenchymal stem cells from chicken bone marrow. Cell and Tissue Banking, 14, 437–51.

    Article  CAS  PubMed  Google Scholar 

  24. Abdallah, B. M., & Kassem, M. (2008). Human mesenchymal stem cells: from basic biology to clinical applications. Gene Therapy, 15, 109–116.

    Article  CAS  PubMed  Google Scholar 

  25. Al-Nbaheen, M., Vishnubalaji, R., Ali, D., Bouslimi, A., Al-Jassir, F., Megges, M., Prigione, A., Adjaye, J., Kassem, M., & Aldahmash, A. (2013). Human stromal (mesenchymal) stem cells from bone marrow, adipose tissue and skin exhibit differences in molecular phenotype and differentiation potential. Stem Cell Reviews, 9(1), 32–43.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Hass, R., Kasper, C., Böhm, S., & Jacobs, R. (2011). Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Communication and Signaling, 9, 12.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Thomson, J., Itskovitz-Eldor, J., Shapiro, S., Waknitz, M., Swiergiel, J., et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science, 282, 1145.

    Article  CAS  PubMed  Google Scholar 

  28. Evans, M. J., & Kaufman, M. H. (1981). Establishment in culture of pluripotential cells from mouse embryos. Nature, 292, 154–156.

    Article  CAS  PubMed  Google Scholar 

  29. Gao, Y., Bai, C., Xiong, H., Li, Q., Shan, Z., Huang, L., Ma, Y., & Guan, W. (2013). Isolation and characterization of chicken dermis-derived mesenchymal stem/progenitor cells. BioMed Research International, 2013(626258), 8.

    Google Scholar 

  30. Pulukuri, S. M., Gorantla, B., Dasari, V. R., Gondi, C. S., & Rao, J. S. (2010). Epigenetic upregulation of urokinase plasminogen activator promotes the tropism of mesenchymal stem cells for tumor cells. Molecular Cancer Research, 8, 1074–1083.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Ahn, J. O., Lee, H. W., Seo, K. W., Kang, S. K., Ra, J. C., & Youn, H. Y. (2013). Anti-tumor effect of adipose tissue derived-mesenchymal stem cells expressing interferon-β and treatment with cisplatin in a xenograft mouse model for canine melanoma. PloS One, 8, e74897.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Joel, M., Sandberg, C. J., Boulland, J. L., Vik-Mo, E. O., Langmoen, I. A., & Glover, J. C. (2013). Inhibition of tumor formation and redirected differentiation of glioblastoma cells in a xenotypic embryonic environment. Developmental Dynamics, 242, 1078–93.

    Article  CAS  PubMed  Google Scholar 

  33. Ma, S., Liang, S., Jiao, H., Chi, L., Shi, X., Tian, Y., Yang, B., & Guan, F. (2014). Human umbilical cord mesenchymal stem cells inhibit C6 glioma growth via secretion of dickkopf-1 (DKK1). Molecular and Cellular Biochemistry, 385(1–2), 277–86.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by Curtin University Commercialization Advisory Board and School of Biomedical Sciences Strategic Research Funds, and India Initiative funds provided by Prof Arun Dharmarajan.

Disclosure of Interest

Authors declare no potential conflicts of interest.

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Authors and Affiliations

  1. Division of Cancer Stem Cells and Cardiovascular Regeneration, Manipal Institute of Regenerative Medicine, Manipal University, Bangalore, 560 065, India

    G Bhuvanalakshmi & Sudha Warrier

  2. School of Biomedical Sciences, Faculty of Health Sciences, Curtin University Perth, Perth, WA, 6845, Australia

    Frank Arfuso, Arun Dharmarajan & Sudha Warrier

  3. School of Anatomy, Physiology and Human Biology, The University of Western Australia, Perth, WA, 6009, Australia

    Frank Arfuso

Authors
  1. G Bhuvanalakshmi
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  2. Frank Arfuso
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  3. Arun Dharmarajan
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  4. Sudha Warrier
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Correspondence to Sudha Warrier.

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Bhuvanalakshmi, G., Arfuso, F., Dharmarajan, A. et al. Multifunctional Properties of Chicken Embryonic Prenatal Mesenchymal Stem Cells- Pluripotency, Plasticity, and Tumor Suppression. Stem Cell Rev and Rep 10, 856–870 (2014). https://doi.org/10.1007/s12015-014-9530-3

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  • DOI: https://doi.org/10.1007/s12015-014-9530-3

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